The Journal of Thoracic and Cardiovascular Surgery
Volume 138, Issue 2 , Pages 374-381 , August 2009

Subtle hemorrhagic brain injury is associated with neurodevelopmental impairment in infants with repaired congenital heart disease

  • Janet S. Soul, MD, CM

      Affiliations

    • Department of Neurology, at Children's Hospital Boston, Boston, Mass
    • Department of Neurology, at Harvard Medical School, Boston, Mass
    • Corresponding Author InformationAddress for reprints: Janet S. Soul, MD, CM, Department of Neurology, Children's Hospital Boston, 300 Longwood Avenue, Boston, MA 02115.
  • ,
  • Richard L. Robertson, MD

      Affiliations

    • Department of Radiology, at Children's Hospital Boston, Boston, Mass
    • Department of Radiology, at Harvard Medical School, Boston, Mass
  • ,
  • David Wypij, PhD

      Affiliations

    • Department of Cardiology, at Children's Hospital Boston, Boston, Mass
    • Department of Pediatrics, at Harvard Medical School, Boston, Mass
    • Department of Biostatistics, Harvard School of Public Health, Boston, Mass
  • ,
  • David C. Bellinger, PhD, MSc

      Affiliations

    • Department of Neurology, at Children's Hospital Boston, Boston, Mass
    • Department of Neurology, at Harvard Medical School, Boston, Mass
  • ,
  • Karen J. Visconti, PhD

      Affiliations

    • Department of Cardiovascular Surgery, at Children's Hospital Boston, Boston, Mass
  • ,
  • Adré J. du Plessis, MBChB, MPH

      Affiliations

    • Department of Neurology, at Children's Hospital Boston, Boston, Mass
    • Department of Neurology, at Harvard Medical School, Boston, Mass
  • ,
  • Barry D. Kussman, MBBCh

      Affiliations

    • Department of Anesthesiology, at Children's Hospital Boston, Boston, Mass
    • Department of Anesthesia, at Harvard Medical School, Boston, Mass
  • ,
  • Lisa A. Scoppettuolo, MS

      Affiliations

    • Department of Cardiology, at Children's Hospital Boston, Boston, Mass
    • Department of Biostatistics, Harvard School of Public Health, Boston, Mass
  • ,
  • Frank Pigula, MD

      Affiliations

    • Department of Cardiovascular Surgery, at Children's Hospital Boston, Boston, Mass
    • Department of Surgery, at Harvard Medical School, Boston, Mass
  • ,
  • Richard A. Jonas, MD

      Affiliations

    • Department of Cardiovascular Surgery, at Children's Hospital Boston, Boston, Mass
    • Department of Surgery, at Harvard Medical School, Boston, Mass
  • ,
  • Jane W. Newburger, MD, MPH

      Affiliations

    • Department of Cardiology, at Children's Hospital Boston, Boston, Mass
    • Department of Pediatrics, at Harvard Medical School, Boston, Mass

Received 1 August 2008 ,Revised 13 November 2008 ,Accepted 9 February 2009.

References 

  1. Bellinger D, Jonas R, Rappaport L, Wypij D, Wernovsky G, Kuban K, et al. Developmental and neurologic status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. N Engl J Med. 1995;332:549–555
  2. Miller G, Tesman J, Ramer J, Baylen B, Myers J. Outcome after open-heart surgery in infants and children. J Child Neurol. 1996;11:49–53
  3. Bellinger DC, Wypij D, Kuban KC, Rappaport LA, Hickey PR, Wernovsky G, et al. Developmental and neurological status of children at 4 years of age after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. Circulation. 1999;100:526–532
  4. Bellinger DC, Bernstein JH, Kirkwood MW, Rappaport LA, Newburger JW. Visual-spatial skills in children after open-heart surgery. J Dev Behav Pediatr. 2003;24:169–179
  5. Bellinger DC, Wypij D, duDuplessis AJ, Rappaport LA, Jonas RA, Wernovsky G, et al. Neurodevelopmental status at eight years in children with dextro-transposition of the great arteries: the Boston Circulatory Arrest Trial. J Thorac Cardiovasc Surg. 2003;126:1385–1396
  6. Karl TR, Hall S, Ford G, Kelly EA, Brizard CP, Mee RB, et al. Arterial switch with full-flow cardiopulmonary bypass and limited circulatory arrest: neurodevelopmental outcome. J Thorac Cardiovasc Surg. 2004;127:213–222
  7. Wernovsky G, Shillingford AJ, Gaynor JW. Central nervous system outcomes in children with complex congenital heart disease. Curr Opin Cardiol. 2005;20:94–99
  8. Majnemer A, Limperopoulos C, Shevell M, Rosenblatt B, Rohlicek C, Tchervenkov C. Long-term neuromotor outcome at school entry of infants with congenital heart defects requiring open-heart surgery. J Pediatr. 2006;148:72–77
  9. Hsia TY, Gruber PJ. Factors influencing neurologic outcome after neonatal cardiopulmonary bypass: what we can and cannot control. Ann Thorac Surg. 2006;81:S2381–S2388
  10. Kinney HC, Panigrahy A, Newburger JW, Jonas RA, Sleeper LA. Hypoxic-ischemic brain injury in infants with congenital heart disease dying after cardiac surgery. Acta Neuropathol (Berl). 2005;110:563–578
  11. Mahle WT, Tavani F, Zimmerman RA, Nicolson SC, Galli KK, Gaynor JW, et al. An MRI study of neurological injury before and after congenital heart surgery. Circulation. 2002;106(12 Suppl. 1):I109–I114
  12. Galli KK, Zimmerman RA, Jarvik GP, Wernovsky G, Kuypers MK, Clancy RR, et al. Periventricular leukomalacia is common after neonatal cardiac surgery. J Thorac Cardiovasc Surg. 2004;127:692–704
  13. McQuillen PS, Hamrick SE, Perez MJ, Barkovich AJ, Glidden DV, Karl TR, et al. Balloon atrial septostomy is associated with preoperative stroke in neonates with transposition of the great arteries. Circulation. 2006;113:280–285
  14. McQuillen PS, Barkovich AJ, Hamrick SE, Perez M, Ward P, Glidden DV, et al. Temporal and anatomic risk profile of brain injury with neonatal repair of congenital heart defects. Stroke. 2007;38(2 Suppl):736–741
  15. du Plessis AJ, Jonas RA, Wypij D, Hickey PR, Riviello J, Wessel DL, et al. Perioperative effects of alpha-stat versus pH-stat strategies for deep hypothermic cardiopulmonary bypass in infants. J Thorac Cardiovasc Surg. 1997;114:991–1001
  16. Jonas RA, Wypij D, Roth SJ, Bellinger DC, Visconti KJ, du Plessis AJ, et al. The influence of hemodilution on outcome after hypothermic cardiopulmonary bypass: results of a randomized trial in infants. J Thorac Cardiovasc Surg. 2003;126:1765–1774
  17. Newburger JW, Wypij D, Bellinger DC, du Plessis AJ, Kuban KC, Rappaport LA, et al. Length of stay after infant heart surgery is related to cognitive outcome at age 8 years. J Pediatr. 2003;143:67–73
  18. Wypij D, Newburger JW, Rappaport LA, duPlessis AJ, Jonas RA, Wernovsky G, et al. The effect of duration of deep hypothermic circulatory arrest in infant heart surgery on late neurodevelopment: the Boston Circulatory Arrest Trial. J Thorac Cardiovasc Surg. 2003;126:1397–1403
  19. Tabbutt S, Nord AS, Jarvik GP, Bernbaum J, Wernovsky G, Gerdes M, et al. Neurodevelopmental outcomes after staged palliation for hypoplastic left heart syndrome. Pediatrics. 2008;121:476–483
  20. Newburger JW, Jonas RA, Soul J, Kussman BD, Bellinger DC, Laussen PC, et al. Randomized trial of hematocrit 25% versus 35% during hypothermic cardiopulmonary bypass in infant heart surgery. J Thorac Cardiovasc Surg. 2008;135:347–354354.e1-4
  21. Maier SE, Gudbjartsson H, Patz S, Hsu L, Lovblad KO, Edelman RR, et al. Line scan diffusion imaging: characterization in healthy subjects and stroke patients. AJR Am J Roentgenol. 1998;171:85–93
  22. Tavani F, Zimmerman RA, Clancy RR, Licht DJ, Mahle WT. Incidental intracranial hemorrhage after uncomplicated birth: MRI before and after neonatal heart surgery. Neuroradiology. 2003;45:253–258
  23. Glauser T, Rorke L, Weinberg P, Clancy R. Acquired neuropathologic lesions associated with the hypoplastic left heart syndrome. Pediatrics. 1990;85:991–1000
  24. Majnemer A, Limperopoulos C, Shevell M, Rohlicek C, Rosenblatt B, Tchervenkov C. Developmental and functional outcomes at school entry in children with congenital heart defects. J Pediatr. 2008;153:55–60
  25. Miller SP, McQuillen PS, Hamrick S, Xu D, Glidden DV, Charlton N, et al. Abnormal brain development in newborns with congenital heart disease. N Engl J Med. 2007;357:1928–1938
  26. Barkovich AJ, Kjos BO, Jackson DE, Norman D. Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology. 1988;166(1 Pt 1):173–180
  27. Partridge SC, Vigneron DB, Charlton NN, Berman JI, Henry RG, Mukherjee P, et al. Pyramidal tract maturation after brain injury in newborns with heart disease. Ann Neurol. 2006;59:640–651
  28. Haacke EM, Xu Y, Cheng YC, Reichenbach JR. Susceptibility weighted imaging (SWI). Magn Reson Med. 2004;52:612–618

 Supported by grants HL 063411 and RR 02172 from the National Institutes of Health.

 Registered with clinicaltrials.gov (#) NCT00006183.

 Dr Jonas is currently Chief of Cardiovascular Surgery and Co-Director of the Children's National Heart Institute, Washington, DC.

PII: S0022-5223(09)00331-6

doi: 10.1016/j.jtcvs.2009.02.027

The Journal of Thoracic and Cardiovascular Surgery
Volume 138, Issue 2 , Pages 374-381 , August 2009